Hyper-activation of Notch3 amplifies the proliferative potential of rhabdomyosarcoma cells

PLoS One. 2014 May 5;9(5):e96238. doi: 10.1371/journal.pone.0096238. eCollection 2014.

Abstract

Rhabdomyosarcoma (RMS) is a pediatric myogenic-derived soft tissue sarcoma that includes two major histopathological subtypes: embryonal and alveolar. The majority of alveolar RMS expresses PAX3-FOXO1 fusion oncoprotein, associated with the worst prognosis. RMS cells show myogenic markers expression but are unable to terminally differentiate. The Notch signaling pathway is a master player during myogenesis, with Notch1 activation sustaining myoblast expansion and Notch3 activation inhibiting myoblast fusion and differentiation. Accordingly, Notch1 signaling is up-regulated and activated in embryonal RMS samples and supports the proliferation of tumor cells. However, it is unable to control their differentiation properties. We previously reported that Notch3 is activated in RMS cell lines, of both alveolar and embryonal subtype, and acts by inhibiting differentiation. Moreover, Notch3 depletion reduces PAX3-FOXO1 alveolar RMS tumor growth in vivo. However, whether Notch3 activation also sustains the proliferation of RMS cells remained unclear. To address this question, we forced the expression of the activated form of Notch3, Notch3IC, in the RH30 and RH41 PAX3-FOXO1-positive alveolar and in the RD embryonal RMS cell lines and studied the proliferation of these cells. We show that, in all three cell lines tested, Notch3IC over-expression stimulates in vitro cell proliferation and prevents the effects of pharmacological Notch inhibition. Furthermore, Notch3IC further increases RH30 cell growth in vivo. Interestingly, knockdown of Notch canonical ligands JAG1 or DLL1 in RMS cell lines decreases Notch3 activity and reduces cell proliferation. Finally, the expression of Notch3IC and its target gene HES1 correlates with that of the proliferative marker Ki67 in a small cohort of primary PAX-FOXO1 alveolar RMS samples. These results strongly suggest that high levels of Notch3 activation increase the proliferative potential of RMS cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cell Line, Tumor
  • Cell Proliferation*
  • Gene Expression Regulation, Neoplastic*
  • Humans
  • Ki-67 Antigen / genetics
  • Ki-67 Antigen / metabolism
  • Oncogene Proteins, Fusion / biosynthesis
  • Oncogene Proteins, Fusion / genetics
  • Paired Box Transcription Factors / biosynthesis
  • Paired Box Transcription Factors / genetics
  • Receptor, Notch1 / genetics
  • Receptor, Notch1 / metabolism
  • Receptor, Notch3
  • Receptors, Notch / genetics
  • Receptors, Notch / metabolism*
  • Rhabdomyosarcoma, Alveolar / genetics
  • Rhabdomyosarcoma, Alveolar / metabolism*
  • Rhabdomyosarcoma, Alveolar / pathology
  • Rhabdomyosarcoma, Embryonal / genetics
  • Rhabdomyosarcoma, Embryonal / metabolism*
  • Rhabdomyosarcoma, Embryonal / pathology
  • Signal Transduction*

Substances

  • Ki-67 Antigen
  • NOTCH1 protein, human
  • NOTCH3 protein, human
  • Oncogene Proteins, Fusion
  • PAX3-FOXO1A fusion protein, human
  • Paired Box Transcription Factors
  • Receptor, Notch1
  • Receptor, Notch3
  • Receptors, Notch

Grants and funding

This work was partially supported by grants from AIRC (Associazione Italiana Ricerca sul Cancro) project #10338 and Ricerca Corrente (Ministero della Salute) to RR; AIRC (progetto speciale 5xmille), MIUR (Ministero dell'Istruzione, Università e della Ricerca, progetto di rilevante interesse nazionale, PRIN) and Ricerca Corrente (Ministero della Salute) to FL; NCI (National Cancer Institute) P01 1666009 to LM and AP. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.